Skip to main content

Characterization of the Microcystis Bloom and Its Nitrogen Supply in San Francisco Estuary Using Stable Isotopes

Abstract

A suite of particulate and dissolved organic and inorganic stable isotopes were needed to determine the source of the nutrients and cells that initiate and sustain the toxic cyanobacteria bloom of Microcystis in San Francisco Estuary. Particulate and dissolved inorganic and organic matter in water and plankton samples were collected biweekly during Microcystis blooms in 2007 and 2008. Stable isotopes for particulate and dissolved organic matter, nitrate, and water (POM-δ 13C, POM-δ 15N, DOC-δ 13C, C/N ratio, NO3-δ 15N, NO3-δ 18O, H2O-δ 18O and H2O-δ 2H) were compared with Microcystis cell abundance, dissolved organic carbon, chlorophyll a, and toxic total microcystins concentration, as well as physical and chemical water quality variables, including streamflow. The isotopic composition of particulate organic matter, nitrate, and water differed for the Sacramento and San Joaquin Rivers and varied along the salinity gradient. The variation of particulate organic matter and water isotopes suggested Microcystis primarily entered the estuary from the San Joaquin and Old Rivers, where it was most abundant. Nitrate isotopes along with streamflow variables indicated that the San Joaquin River was a source of nitrate to the estuary. However, stable isotope comparison of the nitrogen in Microcystis cells with the dissolved inorganic nitrate in the San Joaquin River indicated that nitrate was not the primary source of nitrogen that supported the bloom. Instead, ammonium from the Sacramento River was the likely sole source of the nitrogen for most of the bloom. Selective uptake of ammonium may have further contributed to the magnitude of the Microcystis bloom which increased with the percent of ammonium within the total dissolved inorganic nitrogen pool.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Acuña, S.C., D. Baxa, and S.J. Teh. 2012a. Sublethal dietary effects of microcystin producing Microcystis on threadfin shad, Dorosoma petenense. Toxicon 60: 1191–1202.

    Article  Google Scholar 

  • Acuña, S.C., D.-F. Deng, P.W. Lehman, and S.J. Teh. 2012b. Dietary effects of Microcystis on Sacramento splittail, Pogonichthys macrolepidotus. Aquatic Toxicology 110–111: 1–8.

    Article  Google Scholar 

  • American Public Health Association, American Water Works Association, Water Environment Association. 1998. Standard methods for the examination of water and wastewater, 20th ed. Washington, D.C., USA: American Public Health Association.

    Google Scholar 

  • Boyer, G.L. 2007. The occurrence of cyanobacterial toxins in New York Lakes: Lessons from the MERHAB-Lower Great lakes program. Lake and Reservoir Management 23: 153–160.

    Article  Google Scholar 

  • Canuel, E.A., and J.E. Cloern. 1995. Molecular and isotopic tracers used to examine sources of organic matter and its incorporation into the food webs of San Francisco Bay. Limnology and Oceanography 40: 67–81.

    CAS  Article  Google Scholar 

  • Casciotti, K.L., D.M. Sigman, M. Galanter-Hastings, J.K. Böhlke, and A. Hilkert. 2002. A bacterial method for the measurement of the oxygen isotope composition of nitrate in marine and fresh waters. Analytical Chemistry 74: 4905–4912.

    CAS  Article  Google Scholar 

  • Chaffin, J.D., T.B. Bridgeman, S.A. Heckathorn, and S. Mishra. 2011. Assessment of Microcystis growth rate potential and nutrient status across a trophic gradient in western Lake Erie. Journal of Great Lakes Research 37: 92–100.

    CAS  Article  Google Scholar 

  • Chang, C.C.Y., C. Kendall, S.R. Silva, W.A. Battaglin, and D.H. Campbell. 2002. Nitrate stable isotopes: Tools for determining nitrate sources among different land uses in the Mississippi River Basin. Canadian Journal of Fisheries and Aquatic Science 59: 1874–1885.

    CAS  Article  Google Scholar 

  • Cifuentes, L.A., M.L. Fogel, J.R. Pennock, and J.H. Sharp. 1989. Biogeochemical factors that influence the stable nitrogen isotope ratio of dissolved ammonium in the Delaware Estuary. Geochimica et Cosmochimica Acta 53: 2713–2721.

    CAS  Article  Google Scholar 

  • Clarke, K.R. and R.N. Gorley. 2006. PRIMER v6: User manual/tutorial. PRIMER-E, Plymouth.

  • Cloern, J.E., E.A. Canuel, and D. Harris. 2002. Stable carbon and nitrogen isotope composition of aquatic and terrestrial plants of the San Francisco Bay estuarine system. Limnology Oceanography 47: 713–729.

    CAS  Article  Google Scholar 

  • Dugdale, R.C., F.P. Wilkerson, V.E. Hogue, and A. Marchi. 2007. The role of ammonium in spring bloom development in San Francisco Bay. Estuarine, Coastal and Shelf Science 73: 17–29.

    Article  Google Scholar 

  • Finlay, J.C., and C. Kendall. 2007. Stable isotope tracing of temporal and spatial variability in organic matter sources to freshwater ecosystems. In Stable isotopes in ecology and environmental science, 2nd ed, ed. R.H. Michener and K. Lajtha, 283–333. Malden: Blackwell.

    Chapter  Google Scholar 

  • Ger, K.A., S.J. Teh, D.V. Baxa, S. Lesmeister, and C.R. Goldman. 2010. The effects of dietary Microcystis aeruginosa and microcystin on the copepods of the upper San Francisco Estuary. Freshwater Biology 55: 1548–1559.

    Article  Google Scholar 

  • Glibert, P.M. 2012. Ecological stoichiometry and its implications for aquatic ecosystem sustainability. Current Opinion in Environmental sustainability 4: 272–277.

    Article  Google Scholar 

  • Gu, B., and C.L. Schelske. 1996. Temporal and spatial variations in phytoplankton carbon isotopes in a polymictic subtropical lake. Journal of Plankton Research 18: 2081–2092.

    Article  Google Scholar 

  • Gu, B., A.D. Chapman, and C.L. Schelske. 2006. Factors controlling seasonal variations in stable isotope composition of particulate organic matter in a soft water eutrophic lake. Limnology and Oceanography 5: 2837–2848.

    Article  Google Scholar 

  • Hoffman, J.C., and D.A. Bronk. 2006. Interannual variation in stable carbon and nitrogen isotope biogeochemistry of the Mattaponi River, Virginia. Limnology and Oceanography 51: 2319–2332.

    CAS  Article  Google Scholar 

  • Huang, W.-J., C.-H. Lai, and C.-H. Cheng. 2007. Evaluation of extracellular products and mutagenicity in cyanobacteria cultures separated from a eutrophic reservoir. Science of the Total Environment 377: 214–223.

    CAS  Article  Google Scholar 

  • Ibelings, B.W., and K.E. Havens. 2008. Cyanobacterial toxins: a qualitative meta-analysis of concentrations, dosage and effects in freshwater estuarine and marine biota. Advances in Experimental Medicine and Biology 619: 675–732.

    CAS  Article  Google Scholar 

  • International Agency for Research on Cancer. 2006. Carcinogenicity of nitrate, nitrite and cyanobacterial peptide toxins. The Lancet Oncology 7: 628–629.

    Article  Google Scholar 

  • Jacoby, J.M., E.B. Collier, D.C. Welch, F.J. Hardy, and M. Crayton. 2000. Environmental factors associated with a toxic bloom of Microcystis aeruginosa. Canadian Journal of Fisheries and Aquatic Science 57: 231–240.

    Article  Google Scholar 

  • Jassby, A. 2008. Phytoplankton in the Upper San Francisco Estuary: Recent biomass trends, their causes and their trophic significance. San Francisco Estuary and Watershed Science 6(1), Article 2.

  • Jia, X., D. Shi, R. Kang, H. Li, Y. Liu, Z. An, S. Wang, D. Song and G. Du. 2008. Allelopathic inhibition by Scenedesmus obliquus of photosynthesis and growth of Microcystis aeruginosa. In The 14th international congress on photosynthesis, photosynthesis energy from the Sun, eds. J. F. Allen, E. Gantt, J. H. Golbeck and B. Osmond, 1339–1342. Springer.

  • Kendall, C., and T.B. Coplen. 2001. Distribution of oxygen-18 and deuterium in river waters across the United States. Hydrological Processes 15: 1363–1393.

    Article  Google Scholar 

  • Kendall, C., E. M. Elliott and S. D. Wankel. 2007. Tracing anthropogenic inputs of nitrogen to ecosystems. In Stable isotopes in ecology and environmental science, eds. R.H. Michener and K. Lajtha, 375–449. Blackwell Publishing.

  • Kendall, C., S.R. Silva, and V.J. Kelly. 2001. Carbon and nitrogen isotopic compositions of particulate organic matter in four large river systems across the United States. NASQAN Special Issue Hydrological Processes 15: 1301–1346.

    Article  Google Scholar 

  • Kratzer, C.R., P.D. Dileanis, C. Zamora, S.R. Silva, C. Kendall, B.A. Bergamaschi and R. A. Dahlgren. 2004. Sources and transport of nutrients, organic carbon, and chlorophyll-a in the San Joaquin River upstream of Vernalis, California, during summer and fall, 2000 and 2001. USGS WRI 03–4127. Online: http://water.usgs.gov/pubs/wri/wri034127/.

  • Kraus, T.E.C., B.A. Bergamaschi, P.J. Hernes, R.G.M. Spencer, R. Stepanauskas, C. Kendall, R.F. Losee, and R. Fujii. 2008. Assessing the contribution of wetlands and subsided islands to dissolved organic matter and disinfection byproduct precursors in the Sacramento–San Joaquin River Delta: A geochemical approach. Organic Geochemistry 39: 1302–1318.

    CAS  Article  Google Scholar 

  • Lehman, P.W., J. Sevier, J. Giuliannotti, and M. Johnson. 2004. Sources of oxygen demand in the lower San Joaquin River, California. Estuaries 27: 405–418.

    CAS  Article  Google Scholar 

  • Lehman, P.W., G. Boyer, C. Hall, S. Waller, and K. Gehrts. 2005. Distribution and toxicity of a new colonial Microcystis aeruginosa bloom in the San Francisco Bay Estuary, California. Hydrobiologia 541: 87–90.

    CAS  Article  Google Scholar 

  • Lehman, P.W., G.L. Boyer, M. Satchwell, and S. Waller. 2008. The influence of environmental conditions on the seasonal variation of Microcystis abundance and microcystins concentration in San Francisco Estuary. Hydrobiologia 600: 187–204.

    CAS  Article  Google Scholar 

  • Lehman, P.W., S.J. Teh, G.L. Boyer, M. Nobriga, E. Bass, and C. Hogle. 2010. Initial impacts of Microcystis on the aquatic food web in the San Francisco Estuary. Hydrobiologia 637: 229–248.

    CAS  Article  Google Scholar 

  • Lehman, P.W., K. Marr, G.L. Boyer, S. Acuna, and S.J. Teh. 2013. Long-term trends and causal factors associated with Microcystis abundance and toxicity in San Francisco Estuary and implications for climate change impacts. Hydrobiologia 718: 141–158.

    CAS  Article  Google Scholar 

  • Lehmann, M.F., S.M. Bernasconi, J.A. McKenzie, A. Barbieri, M. Simona, and M. Veronesi. 2004. Seasonal variation of the δ 13C and δ 15N of particulate and dissolved carbon and nitrogen in Lake Lugano: Constraints on biogeochemical cycling in a eutrophic lake. Limnology and Oceanography 49: 415–429.

    CAS  Article  Google Scholar 

  • Lis, G., L.I. Wassenaar, and M.J. Hendry. 2008. High precision laser spectroscopy D/H and 18O/16O measurements of microliter natural water samples. Analytical Chemistry 80: 287–293.

    CAS  Article  Google Scholar 

  • Lurling, M. 2003. Daphnia growth on microcystin-producing and microcystin-free Microcystis aeruginosa in different mixtures with the green alga Scenedesmus. Limnology and Oceanography 48: 2214–2220.

    Article  Google Scholar 

  • Martineau, C., W.F.V. Martineau, J.-J. Frenette, and J.J. Dodson. 2004. Primary consumers and particulate organic matter: Isotopic evidence of strong selectivity in the estuarine transition zone. Limnology and Oceanography 49: 1679–1686.

    CAS  Article  Google Scholar 

  • Mayer, B., E.W. Boyer, C. Goodale, N.A. Jaworski, N. Van Breemen, R.W. Howarth, S. Seitzinger, G. Billen, K. Lajtha, K. Nadelhoffer, D. Van Dam, L.J. Hetling, M. Nosal, and K. Paustia. 2002. Sources of nitrate in rivers draining sixteen watersheds in the northeastern U.S.: Isotopic constraints. Biogeochemistry 57(58): 171–197.

    Article  Google Scholar 

  • Moisander, P.H., P.W. Lehman, M. Ochiai, and S. Corum. 2009. Diversity of the toxic cyanobacterium Microcystis aeruginosa in the Klamath River and San Francisco Bay delta, California. Aquatic Microbial Ecology 57: 19–31.

    Article  Google Scholar 

  • Panno, S.V., K.C. Hackley, W.R. Kelly, and H.-H. Hwang. 2006. Isotopic evidence of nitrate sources and denitrification in the Mississippi River, Illinois. Journal of Environmental Quality 35: 495–504.

    CAS  Article  Google Scholar 

  • Parker, A.E., V.E. Hogue, F.P. Wilkerson, and R.C. Dugdale. 2012. The effect of inorganic nitrogen speciation on primary production in San Francisco Estuary. Estuarine, Coastal and Shelf Science 104–105: 91–101.

    Article  Google Scholar 

  • SAS Institute, Inc. 2013. SAS/STAT 12.3 user’s guide. Cary, NC: SAS Institute Inc.

    Google Scholar 

  • Sebilo, M., G. Billen, B. Mayer, D. Billiou, M. Grably, J. Garnier, and A. Mariotti. 2006. Assessing nitrification and denitrification in the Seine River and Estuary using chemical and isotopic techniques. Ecosystems 9: 564–577.

    CAS  Article  Google Scholar 

  • Sedmak, B., and T. Eleršek. 2006. Microcystins induce morphological and physiological changes in selected representative phytoplanktons. Microbial Ecology 5: 508–515.

    Article  Google Scholar 

  • Sedmak, B., and G. Kosi. 1998. The role of microcystins in heavy cyanobacterial bloom formation. Journal of Plankton Research 20: 691–708.

    CAS  Article  Google Scholar 

  • Sieracki, C.K., M.E. Sieracki, and C.S. Yentsch. 1998. An imaging-in-flow system for automated analysis of marine microplankton. Marine Ecololgy and Progress Series 168: 285–296.

    Article  Google Scholar 

  • Sigman, D.M., K.L. Casciotti, M. Andreani, and C. Barford. 2001. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Analytical Chemistry 73: 4145–4153.

    CAS  Article  Google Scholar 

  • Singh, D.P., M.B. Fyagi, A. Kumar, and J.K. Thakur. 2001. Antialgal activity of a hepatotoxin-producing cyanobacterium, Microcystis. World Journal of Microbiology and Biotechnology 17: 15–22.

    CAS  Article  Google Scholar 

  • Sommer, T.R., C. Armor, R. Baxter, R. Breuer, L. Brown, M. Chotkowski, S. Culberson, F. Feyrer, M. Gingras, B. Herbold, W. Kimmerer, A. Mueller-solger, M. Nobriga, and K. Souza. 2007. The collapse of pelagic fishes in the upper San Francisco Estuary. Fisheries 32: 270–277.

    Article  Google Scholar 

  • Spiker, E. C. and L. E. Shemel. 1979. Distribution and stable isotope composition of organic carbon in San Francisco Bay. In San Francisco Bay: The urbanized Eestuary, ed. J. Conomos, 195–212. Pacific Division American Association for the Advancement of Science.

  • St. Jean, G. 2003. Automated quantitative and isotopic (13C) analysis of dissolved inorganic carbon and dissolved organic carbon in continuous-flow using a total organic carbon analyzer. Rapid Communications in Mass Spectrometry 17: 419–428.

    CAS  Article  Google Scholar 

  • Takamura, N., T. Iwakuma, and M. Yasuno. 1987. Uptake of 13C and 15 N (ammonium, nitrate and urea) by Microcystis in Lake Kasumigaura. Journal of Plankton Research 9: 151–165.

    Article  Google Scholar 

  • United States Environmental Protection Agency. 1983. Methods for chemical analysis of water and wastes. Technical Report EPA-600/4-79-020. United States Environmental Protection Agency, Washington, DC, USA.

  • United States Geological Survey. 1985. Methods for determination of inorganic substances in water and fluvial sediments. Open File Report 85–495.

  • Vassilakaki, M., and S. Pflugmacher. 2008. Oxidative stress response of Synechocystis sp. (PCC 6803) due to exposure to microcystin-LR and cell-free cyanobacterial crude extract containing microcystin-LR. Journal of Applied Phycology 20: 219–225.

    CAS  Article  Google Scholar 

  • Vuorio, K., M. Meili, and J. Sarvala. 2006. Taxon-specific variation in the stable isotopic signatures (δ 13C and δ 15N) of lake phytoplankton. Freshwater Biology 51: 807–822.

    CAS  Article  Google Scholar 

  • Wankel, S.D., C. Kendall, C.A. Francis, and A. Paytan. 2006. Nitrogen sources and cycling in the San Francisco Bay Estuary: A nitrate dual isotope approach. Limnology and Oceanography 51: 1654–1664.

    CAS  Article  Google Scholar 

  • Wankel, S.D., C. Kendall, J.T. Pennington, F.P. Chavez, and A. Paytan. 2007. Nitrification in the euphotic zone as evidenced by nitrate dual isotopic composition: Observations from Monterey Bay, California. Global Biogeochemial Cycles 21: 3–13.

    Google Scholar 

  • Wankel, S.D., C. Kendall, and A. Paytan. 2009. Using nitrate dual isotopic composition (δ 15N and δ 18O) as a tool for exploring sources and cycling of nitrate in an estuarine system: Elkhorn Slough, CA. Journal of Geophysical Research 114, G01011. doi:10.1029/2008JG000729.

    Article  Google Scholar 

  • Xu, J., M. Zhang, and P. Xie. 2007. Stable carbon isotope variations in surface bloom scum and subsurface seston among shallow eutrophic lakes. Harmful Algae 6: 679–685.

    CAS  Article  Google Scholar 

  • Yang, Z., F. Kong, X. Shi, M. Zhang, P. Xing, and H. Cao. 2008. Changes in the morphology and polysaccharide content of Microcystis aeruginosa (cyanobacteria) during flagellate grazing. Journal of Phycology 44: 716–720.

    Article  Google Scholar 

  • Yoshida, M., T. Togashi, K. Takeya, J. Yoshimura, and M. Tatsuo. 2007. Ammonium supply mode and the competitive interaction between the cyanobacterium Microcystis novacekii and the green alga Scenedesmus quadricauda. Fundam. Applied Limnology 170: 133–140.

    Article  Google Scholar 

  • Zegura, B., B. Sedmak, and M. Filipi. 2003. Microcystin-LR induces oxidative DNA damage in human hepatoma cell line HepG2. Toxicon 41: 41–48.

    CAS  Article  Google Scholar 

Download references

Acknowledgements

Funding for this research was provided through a Delta Science grant to Drs. Lehman, Boyer and Teh with additional financial and facilities assistance from the California Department of Water Resources, UC Davis, the U. S. Geological Survey, and the U.S. Fish and Wildlife Service. We also thank the reviewers for their careful review of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. W. Lehman.

Additional information

Communicated by Hans W. Paerl

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lehman, P.W., Kendall, C., Guerin, M.A. et al. Characterization of the Microcystis Bloom and Its Nitrogen Supply in San Francisco Estuary Using Stable Isotopes. Estuaries and Coasts 38, 165–178 (2015). https://doi.org/10.1007/s12237-014-9811-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-014-9811-8

Keywords

  • Microcystis
  • Stable isotopes
  • Nutrients
  • Cyanobacteria bloom
  • Estuary
  • Streamflow